PROPOSED CHANGES TO THE CLASSIFICATION SYSTEM OF
LIVING COCCOLITHOPHORIDS. Ill.
Ric W. Jordan, Institute of Oceanographic Sciences, Wormley, Surrey , UK
Annelies Kleijne, Institute for Earth Sciences, Vrije Universiteit, Amsterdam, NL
Berit R. Heimdal, Dept .of Fisheries and Marine Biology, University of Bergen, Norway
The classification of living coccolithophorids is presently under further scrutiny following therecent review by Jordan & Kleijne (in press). This has been initiated, in particular, by the needs oftwo ambitious projects, The Encyclopedia of Algal Genera (ed. B.C. Parker) and the ExpertCentre for Taxonomic Identification (ETI). As a cor-sequence of their requests for information it
has been necessary to re-examine, and in some cases revise, the generic concepts of a number oftaxa, and to provide an up-to-date list of all known species (Jordan & Green, 1993). In this paper
we discuss the new combinations of several species previously assigned to Cricosphaera, a genus
regarded as a junior synonym of Pleurochrysis.
Also we propose that, where holococcolith and heterococcolith bearing species are shown
to be alternate phases of a single life-cycle, the two phases should be recombined as one species,
but with each phase assigned forma status.
TAXONOMIC RECOMMENDATIONSCalyptrolithina divergens var. tuberosa (Heimdal, in Heimdal & Gaarder 1980) stat. nov. (Note1)

Basionym: Zygosphaera divergens f. tuberosa Heimdal, in Heimdal & Gaarder, 1980,
p.l2, p1.3, fig.25.
Synonym: Calyptrolithina divergens f. tuberosa (Heimdal, in Heimdal & Gaarder)
Heimdal, 1982, p.54.
Papposphaera borealis f. sagittifera (Manton et al1916) comb. & stat. nov. (Note 2)
Basionym: Papposphaera sagittifera Manton., Sutherland, & McCully 1976, pp.228-229,figs 14.
·Synonym: Papposphaera borealis (Manton, Sutherland & Oates 1976) Thomsen,0stergaard & Hansen, 1991, p.641, figs 2-4, 9 (in part).
Papposphaera arctica f. sarion (Thomsen 1981) comb. & stat. nov. (Note 2)
Basionym: Papposphaera sarion Thomsen, 1981, p.79, figs 5-8.
Synonym: Papposphaera arctica (Manton, Sutherland & Oates) Thomsen, 0stergaard &Hansen, 1991, pp.640-641, figs 5-8 (in part).
Pleurochrysis elongata (Droop 1955) comb. nov. (Note 3)
Basionym: Syracosphaera (Hymenomonas) elongata Droop, 1955, p.240, figs 12-14.
Synonyms: Cricosphaera elongata (Droop) Braarud, 1960, p.212.
Hymenomonas elongata (Droop) Parke & Green, 1976, pp.552 and 554.
Pleurochrysis gayraliae (Beuffe 1978) comb. nov. (Note 3)
Basionym: Cricosphaera gayraliae Beuffe, 1978, p.458, figs 1-13.
Scyphosphaera apsteinii var. dilatata (Gaarder 1970) stat. nov. (Note 1)
Basionym: Scyphosphaera apsteinii f. dilatata Gaarder, 1970, p.119, figs 4-6.
Syracosphaera dilatata (Heimdal, in Heimdal & Gaarder 1981) stat. nov. (Note 4)
Basionym: Caneosphaera halldalii f. dilatata Heimdal, in Heimdal & Gaarder, 1981,p.44, pl.2, fig.9.
Synonym: Syracosphaera halldalii f. dilatata (Heimdal, in Heimdal & Gaarder) Jordan& Young, 1990, pp.15-16.

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INA Newsletter 15/1 - 1993

Tetralithoides Theodoridis 1984 emend.
Type species: Tetralithoides quadrilaminata (Okada & Mcintyre) comb. nov.
Emended description: Coccosphere shape unknown, but with monomorphic oval
coccoliths. Each coccolith rim bearing both a proximal and distal flange of equalsize. Rim surrounding a large central area, with calcified plates covering the proximal
part of the coccolith.
Type species: Tetralithoides quadrilaminata (Okada & Mcintyre) comb. nov.
Tetralithoides quadrilllminata (Okada & Mclntyre 1977) comb. nov. (Note 5 & Figs 1-2)
Basionym: Cricosphaera quadrilaminata Okada & Mcintyre 1977, p.15, pl.6, figs 5-6.
Synonym: Tetralithoides symeonidesii Theodoridis, 1984, p.88, pl.9, figs 5-12.
Emended description: Oval caneolith-like coccoliths with a very large central area coveredby three or four angular plates forming a solid bottom. Central plates interlock in acomplicated manner in distal view. In proximal view plates appear fused giving X- orY -shaped suture lines. Distal and proximal flanges similar in size. Proximal part ofrim with a short oblique continuation directed into the central area and overlying thecentral area plates. Coccoliths 3.9 to 7.5 J.Lm long and 2.9 to 5.2 !Jm wide.
EXPLANATORY NOTES
1) Use of varieties. In a previous paper the use of subspecies in coccolithophorid taxonomy wasdiscussed and it was proposed that use of variety was generally preferable (Jordan & Young,1990). At that time taxa of forma status were not mentioned. Since then there has been a proposal
to adopt forma' status exclusively for the use of life cycle stages (Kleijne, 1991 ). This proposal issupported and continued below (see Note 2). However, within the classification scheme there are
two taxa with forma status which are not alternate life cycle stages of the type form. To avoid
future confusion it is proposed here to change their status to variety.
2) Heterococcolithophorid/holococcolithophorid combinations within the Papposphaeraceae.
Recently, it has been :reported that cells of Papposphaera and Pappomonas spp. were seen tocombine consistently with cells of Turrisphaera and Trigonaspis spp. (Thomsen et al., 1991).
This association, called a "combination cell" (see Thomsen et al., 1991, figs 8 & 9), only occurs
between discrete pairs of species. For instance, Papposphaera sagittifera and Turrisphaera
borealis, Papposphaera sarion and Turrisphaera arctica, Papposphaera sp. and Turrisphaera
polybotrys, and Pappomonas flabellifera var. borealis and Trigonaspis cf. diskoensis. The authors
believed that these associations were part of the life histories of these species. To emphasise thisthey transferred the Turrisphaera species to their Papposphaera counterparts. As the latter genus
has priority Turrisphaera has now become superfluous and a junior synonym of Papposphaera.
However, in the case of two species the new combinations took the specific epithet .of theholococcolithophorid stage (Turrisphaera" phase), as they were described prior to, or at the sametime as, their respective heterococcolithophorid stage. Thus the combinations P. arctica and P.
borealis were created.
In the literature there are only two other examples of heterococcolithophoridholococcolithophorid alternate life cycles. These are Coccolithus pelagicus and 'Crystallolithus'
hyalinus/C. braarudii (Parke & Adams, 1960; Rowson et al., 1986), and Calcidiscus leptoporus
and 'Crystallolithus' rigidus (Kleijne, 1991). However, they do not form combination cells likethose above, instead one stage is produced and subsequently released from inside the cell of theother stage. Furthermore, as recommended by Kleijne (1991) the stages in the life cycle ofcoccolithophorids should be retained as separate taxonomic units with forma status. Thus inaccordance with this recommendation the combinations proposed by Thomsen et al. (1991)
should be further subdivided to this level (see the section on taxonomic recommendations).

3) Assignment of species of Cricosphaera. Braarud (1960) described this genus for mono-morphic cricolith-bearing coccolithophores Braarud ( 1960) transferred two Syracosphaera
species into his new genus; S. carterae and S. elongata. The former was designated as the typespecies and two further species were later added to the genus; C. quadrilaminata (Okada &Mcintyre, 1977) and C. gayraliae (Beuffe, 1978). However, several years earlier Pleurochrysis
had been described by Pringsheim (1955) on the basis of its flagellar morphology and life

INA Newsletter 15/1 - 199319

history, but without any knowledge of its coccoliths. These coccoliths were recognised later ascricoliths. At that time the two genera were separated by life history. Species were only retained in
Cricosphaera if a benthic stage had not been recognised. However, Christensen (1978) transferred C. carterae to Pleurochrysis on the grounds that it possessed a benthic stage. By transferring the type species of Cricosphaera to Pleurochrysis the former became superfluous and ajunior synonym of the latter. Thus the species of Cricosphaera should be transferred toPleurochrysis or to another genus (see Note 5).
4) Syracosphaera dilatata. The taxon was first described as a form of Caneosphaera halldalii byHeimdal and Gaarder (1981) and later transferred to Syracosphaera (Jordan & Young, 1990).

The coccoliths of this form are, however, signi~cantly different from the type, S. halldalii f.
halldalii. The type possesses a distinct, wide distal flange (see Gaarder & Heimdal, 1977, pl.6),
whilst f. dilatata has merely a flared rim (see Heimdal & Gaarder, 1981, pl.2, fig.9). In addition,
the presence of a beaded mid-wall flange on the circum-flagellar coccoliths of f. dilatata, whichis mentioned but not figured by the authors (Heimdal & Gaarder, 1981, p.44 ), is a significant
difference between this form and the type. Neither S. halldalii or its close relative, S. molischii,
have a mid-wall flange. It is therefore proposed to elevate S. halldalii f. dilatata to species level.
5) Tetralithoides quadrilaminata. Cricosphaera quadrilaminata was first described from thedeep photic zone of subtropical/tropical waters of both the Atlantic and Pacific Oceans (Okada &Mcintyre, 1977). Since then it has only been recorded a few times: in deep photic waters of thesubtropical N.E. Atlantic (Jordan & Kleijne, unpubl. obs); in Miocene sediments of theMediterranean, the Atlantic and the Indian Ocean (Theodoridis, 1984); and in Quaternary
sediments of the Philippine Sea (Matsuoka & Okada, 1989) and off the coast of Japan (Okada,1992).
Its coccoliths were described as cricolith-like, however, the possession of calcareous
elements associated with the proximal part of the tube and of other elements filling the central
area (Fig.1), is not characteristic of members of the Pleurochrysidaceae. In our opinion thesecalcified plates may be homologous to the flattened plates of Alisphaera or the radial laths of
Syracosphaera spp. In addition, the oblique continuation of the rim into the central area (Fig.2),
is also a character of both Alisphaera and Syracosphaera spp. (Jordan et al., in prep.). Thus
transfer of this species to Pleurochrysis would not be not as satisfactory as for the other
Cricosphaera species (see Note 3). Its taxonomic position would be more closely associated with
the Syracosphaeraceae. Placement in Alisphaera would not be satisfactory, because the development of the central area in C. quadrilaminata is significantly different.
Theodoridis (1984) described a new genus and species, Tetralithoides symeonidesii, fromthe Miocene of the western Mediterranean (DSDP Site 372). He recorded occurrences from zones
NN2 to NN11. The polarised light micrographs closely resemble the one featured later in Okada(1992), however, Theodoridis did not realise that his new species was identical to Cricosphaera
quadrilaminata (Okada & Mclntyre, 1977) described seven years earlier. We therefore propose
the new combination Tetralithoides quadrilaminata.

ACKNOWLEDGEMENTS
We would like to thank Dr. Tyge Christensen for his advice in matters of the ICBN. We are alsoindebted to Jcremy Young for his comments and criticisms of the manuscript, especially forpointing out the existence and relevance of Theodoridis' paper. The taxonomic position of thePapposphaera sagittifera!Turrisphaera borealis combination cell has been made after consultation with H.A. Thomsen and J.B. 0stergaard.
REFERENCES
Beuffe H. 1978: Une Coccolithophoracee marine nouvelle: Cricosphaera gayraliae nov. sp. Protistologica, 14, 451458.
Braarud T. 1960: On the coccolithophorid genus Cricosphaera n. gen. Nytt Mag. Bot., 8, 211-212.
Christensen T. 1978: Annotations to a textbook of Phycology. Bot. Tidsskrift, 73, 65-70.
Droop M.R. 1955: Some new supra-littoral Protista. J. mar. bioi. Ass. U.K., 34, 233-245.
Gaarder, K.R. 1970: Three new taxa of Coccolithineae. Nytt Mag. Bot., 17, 113-126.
Gaarder, K.R. & Heimdal, B.R. 1977: A revision of the genus Syracosphaera Lohmann (Coccolithineae). "Meteor"
Forsch.-Ergebnisse, Ser.D, 24, 54-71.

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Halldal, P. & Markali, J. 1955: Electron microscope studies on coccolithophorids from the Norwegian Sea, the Gulf
Stream and the Mediterranean. Norske Vidensk. Akad. Oslo, Avh., Math. Nat. Kl., 1, 1-30.
Heimdal B.R. 1982: Validation of the names of some species of Zygosphaera KAMPTNER.INA. Newsletter, 4, 5256.
Heimdal B.R. & Gaarder, K.R. 1980: Co.ccolithophorids from the northern part of the eastern central Atlantic. I.
Holococcolithophorids. "Meteor" Forsch.-Ergebnisse, Ser.D, 32, 1-14.
Heimdal B.R. & Gaarder K.R. 1981: Coccolithophorids from the northern part of the eastern central Atlantic. IT. Heterococcolithophorids. "Meteor" Forsch.-Ergebnisse, Ser.D, 33, 37-69.
Jordan R.W. & Green J.C. 1993: A checklist of the Haptophyta. J. mar. biol. Ass. U.K., submitted.
Jordan R.W. & Kleijne A. in press: A classification system for living coccolithophores. In: Coccolithophores, WinterA. & Siesser W.G. (eds), Cambridge University Press, Cambridge.
Jordan R.W. & Young, J.R. 1990: Proposed changes to the classification system of living coccolithophorids. l.N .A.
Newsletter, 12, 15-18.
Kleijne A. 1991: Holococcolithophorids from the Indian Ocean, Red Sea, Mediterranean Sea and North Atlantic Ocean.
Marine Micropaleontology, 17, 1-76.
Manton 1., Sutherland J. & McCully M. 1976: Fine structural observations on coccolithophorids from South Alaska inthe genera Papposphaera Tangen and Pappomonas Manton and Oates. Br. phycol. J., 11, 225-238.
Manton 1., Sutherland J. & Oates K. 1976: Arctic coccolithophorids: two species of Turrisphaera gen. nov. from West
Greenland, Alaska, and the Northwest Passage. Proc. R. Soc. Lond. B., 194, 179-194.
Matsuoka H. & Okada H. 1989: Quantitative analysis of Quaternary nannoplankton in the subtropical Northwestern
Pacific Ocean. Marine Micropaleontology, 14, 97-118.
Okada H. 1992: Biogeographic control of modem nannofossil assemblages in surface sediments of Ise Bay, Mikawa
Bay and Kumano-Nada, off coast of Central Japan. Memorie di Scienze Geologiche, 43, 431-449.
Okada H. & Mclntyre A. 1977: Modern coccolithophores of the Pacific and North Atlantic Oceans.
Micropaleontology, 23, 1-55.
Parke M. & Adams I. 1960: The motile (Crystallolithus hyalinus Gaarder & Markali) and non-motile phases in the life
history of Coccolithus pelagicus (Wallich) Schiller. J. mar. biol. Ass. U.K., 39, 263-274.
Parke M. & Green J.C. 1976: Haptophyta. In: Check-list of British Marine Algae - Third revision, Parke M. & Dixon
P.S. (eds), J. mar. biol. Ass. U.K., 56, 527-594.
Pringsheim E.G. 1955: Kleine Mitteilungen iiber Flagellaten und Algen. I. Algenartige Chrysophyceen in Reinkultur.
Archiv fur Mikrobiologie, 21, 401-410.
Rowson J.D., Leadbeater B.S.C. & Green J.C. 1986: Calcium carbonate deposition in the motile (Crystallolithus)
phase of Coccolithus pelagicus. Br. phycol. J., 21, 359-370.
Theodoridis, S. 1984: Calcareous nannofossil biostratigraphy of the Miocene and revision of the helicoliths anddiscoasters. Utrecht Micropaleontol. Bull., 32, 1-271.
Thomsen H.A. 1981: Identification by electron microscopy of nanop1anktonic coccolithophorids(Prymnesiophyceae) from West Greenland, including the description of Papposphaera sarion sp. nov. Br.
phycol. J., 16, 77-94.
Thomsen H.A., Buck K.R., Coale S.L., Garrison D.L. & Gowing M.M. 1988: Nanoplanktonic coccolithophorids(Prymnesiophyceae, Haptophyceae) from the Weddell Sea, Antarctica. Norw. J. Bot., 8, 419-436.
Thomsen H.A., 0stergaard J.B. & Hansen L.E. 1991: Heteromorphic life histories in arctic coccolithophorids(Prymnesiophyceae). J. Phycol., 27, 634-642.

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I

*PLATE:
figure I . Coccohths of Tetrallthotdes quadnlamtnata showing both dtstal and proxirml views. In distal view the 3 or 4 central area plates are shown
to be overlapping, whilst in proximal view they appear fused in X- or Y- shaped suture lines. Specimen from 160m at St. 11311 (26"11 'N 44°$3 ' W).
2~figure 2: Coccoliths ofTetrallthotdes quadrtlammata showing both distal and proximal views at higher magnification. Note also the smaller obliquecontinuations of the rim at the proxirml end of the tube (arrowed). Bar - 2 fUll·•These photographs were published in the article by R. W. Jordan, A KJeijne & B. R. Heimdal: Proposed changes tothe classification system ofliving coccolithophorids Ill. , INA Newsletter, 15/1, 1993, p. 18- 22 . Due to the bad qualityof printing we reproduce them again.

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